He joined MI6 in 1966 and was posted to Nairobi in 1968.[5] In 1984, he was appointed an OBE. After being posted to Prague, Paris and Geneva, he became head of Washington station in 1991,[5] director of personnel and administration in 1993 and director of operations in 1994.[5] Dearlove became Chief in 1999.[5] In 2001, he was appointed a KCMG.

Sir Richard's tenure as the head of MI6 saw many events for the Service:

Tension with the Government over the evidence for war on Iraq. It has been suggested that many within the intelligence community were uneasy that their qualified judgements on Iraq's weapons of mass destruction were presented as hard facts in various dossiers (e.g. September Dossier). In July 2002, Dearlove told ministers that in the US "intelligence and facts were being fixed around the policy".[6]

In February 2008 Dearlove gave evidence at the inquest of Princess Diana's death, responding to Harrods owner Mohamed al-Fayed who claimed that MI6 had murdered Diana.[5]

Sir Richard is a signatory of the Henry Jackson Society principles.[9] He is also a "senior advisor" to the Monitor Group – a consultancy and private equity firm which has been implicated in undertaking PR work for Libya and Muammar Gaddafi. In April 2013, it was announced that Dearlove joined the advisory board of Ergo, an intelligence and advisory firm.[10]

On 15 February 2011 Dearlove gave a talk at the Cambridge Union Society, taking as his theme the question of how much secrecy the UK needs: "The short answer to that question is that it needs some but actually not as much as you think."[11](2:48) He said he "would definitely draw a parallel at the moment between the wave of political unrest which is sweeping through the Middle East, in a very excited and rather extraordinary fashion, and also the Wikileaks phenomenon",[11](3:25) but added later, in connection with the way technological advances was altering the norms of civic and private life, commenting on WikiLeaks founder Julian Assange, that " ... the Assange story, as such, is ultimately a distraction. He's a very undignified flag-carrier, in my opinion, for a very important issue."[11](11:50)

In 2012 Dearlove took a sabbatical from Cambridge University to write an account of events leading up to the 2003 invasion of Iraq from his perspective at MI6, including coverage of the production of the so-called "dodgy dossier". Publishing such an account would be unprecedented for a former Chief of the Secret Intelligence Service. He may release this now that the Chilcot Inquiry findings have been published.[12]

On 7 July 2014, in a lecture at the Royal United Services Institute, Dearlove argued that the government and media had exaggerated the Islamist terrorism threat to the UK, giving extremists publicity counter-productive to UK interests.[13][14]